The Histochemical Journal

, Volume 28, Issue 4, pp 289–297 | Cite as

Distribution of peptidergic nerve fibres in bullfrog lingual papillae demonstrated by a combination of double immunofluorescence labelling and a multiple dye filter

  • Tatsumi Kusakabe
  • Tadashi Kawakami
  • Michio Ono
  • Hajime Sawada
  • Toshifumi Takenaka
Papers

Summary

Immunoreactivity of substance P, calcitonin gene-related peptide, vasoactive intestinal polypeptide, neuropeptide Y, and galanin is localized in nerve fibres distributed in the fungiform and filiform papillae of the tongue of the bullfrog,Rana catesbeiana. A combination of indirect double immunofluorescence labelling and a multiple dye filter system clearly demonstrated that all substance P fibres in the connective tissue core of the fungiform and filiform papillae, and within the rim of ciliated cells located on the top of the fungiform papillae showed coexistence with calcitonin gene-related peptide. A few fibres in the epithelial discs, which are located in the centre of the top of the fungiform papillae, showed the immunoreactivity of calcitonin gene-related peptide alone. There were no substance P fibres which showed coexistence with vasoactive intestinal polypeptide, galanin, and neuropeptide Y. In high magnification images, substance P and vasoactive intestinal polypeptide, and substance P and galanin fibres were recognized as two interwined fibres within the same thin nerve bundle. No immunoreactivity of leucine- and methionine-enkephalins can be detected.

These findings suggest that the chemoreceptor function of the bullfrog gustatory organ may be under the control of complicated peptidergic innervation.

Keywords

Vasoactive Intestinal Polypeptide Ciliated Cell Nerve Bundle Double Immunofluorescence Labelling High Magnification Image 

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References

  1. Baecker, B., Yanaihara, N. &Forssmann, W.G. (1983) VIP innervation of the tongue in vertebrates.Anat. Embryol. 167, 173–89.CrossRefPubMedGoogle Scholar
  2. Dehan, R.S. &Graziadei, P.P.C. (1971) Functional anatomy of frog's taste organs.Experientia 27, 823–6.CrossRefPubMedGoogle Scholar
  3. Finger, T. E. (1986) Peptide immunohistochemistry demonstrates multiple classes of perigemmal nerve fibers in the circumvallata papilla of the rat.Chem. Senses. 11, 135–44.Google Scholar
  4. Graziadei, P. P. C. &Dehan, R. S. (1971) The ultrastructure of frog's taste organs.Acta Anat. 80, 563–603.PubMedGoogle Scholar
  5. Hirata, K. &Kanaseki, T. (1987) Substance P-like immunoreactive fibers in the frog taste organs.Experientia 43, 386–9.CrossRefPubMedGoogle Scholar
  6. Ichikawa, H., Nishikawa, S., Wakisaka, S., Matsuo, S., Takano, Y. &Akai, Y. (1988) Coexistence of vasoactive intestinal polypeptide-and substance P-like immunoreactivities in the tongue of the guinea pig.Neurosci. Lett. 89, 283–5.CrossRefPubMedGoogle Scholar
  7. Jaeger, C.B. &Hillman, D.E. (1976) Morphology of gustatory organs. InFrog Neurobiology (edited by R. Llians & W. Precht) pp. 587–606. Heidelberg: Springer-Verlag.Google Scholar
  8. Kawakami, T., Kusakabe, T. &Takenaka, T. (1995) Distribution of immunoreactive neuropeptides in the pancreas of the bullfrog,Rana catesbeiana, demonstrated by immunofluorescence.Cell Tissue Res. 280, 307–11.PubMedGoogle Scholar
  9. Kinnman, E. &Aldskogius, H. (1991) The role of substance P and calcitonin gene-related peptide containing nerve fibers in maintaining fungiform taste buds in the rat after a chronic chorda tympani nerve injury.Exp. Neurol. 113, 85–91.CrossRefPubMedGoogle Scholar
  10. Kline, L.W., Kaneko, T., Chiu, K.W., Harvey, S. &Pang, P.T.K. (1988) Calcitonin gene-related peptide in the bullfrog,Rana catesbeiana: Localization and vascular actions.Gen. Comp. Endocrinol. 72, 123–9.CrossRefPubMedGoogle Scholar
  11. Kuramoto, H. (1988) An immunohistochemical study of cellular and nervous elements in the taste organ of the bullfrog,Rana catesbeiana.Arch Histol. Cytol. 51, 205–21.PubMedGoogle Scholar
  12. Kusakabe, T., Kawakami, T., Hori, H., Bandou, Y. &Takenaka, T. (1993a) Immunohistochemical coexistence of calcitonin gene-related peptide and substance P in the nerve fibers of the internal gills of bullfrog (Rana catesbeiana) larvae.Neurosci. Lett. 158, 59–62.CrossRefPubMedGoogle Scholar
  13. Kusakabe, T., Kawakami, T., Tanabe, Y., Fujii, S., Bandou, Y. &Takenaka, T. (1993b) Coexistence of substance P and calcitonin gene-related peptide in the nerve fibers of the carotid labyrinth of the bullfrog,Rana catesbeiana.Brain Res. 603, 153–6.CrossRefPubMedGoogle Scholar
  14. Kusakabe, T., Kawakami, T. &Takenaka, T. (1994a) Coexistence of substance P, neuropeptide Y, VIP, and CGRP in the nerve fibers of the carotid labyrinth of the bullfrog,Rana catebeiana: a double-labelling immunofluorescence study in combination with alternate consecutive sections.Cell Tissue Res. 276, 91–7.CrossRefPubMedGoogle Scholar
  15. Kusakabe, T., Kawakami, T. &Takenaka, T. (1994b) Localization of immunoreactive neuropeptides in the kidney of the bullfrog,Rana catesbeiana, by immunofluorescence.Cell Tissue Res. 278, 41–4.PubMedGoogle Scholar
  16. Kusakabe, T., Kawakami, T. &Takenaka, T. (1995a) Peptidergic innervation in the amphibian carotid labyrinth.Histol. Histopathol. 10, 185–202.PubMedGoogle Scholar
  17. Kusakabe, T., Kawakami, T., Ono, M., Hori, H., Sawada, H. &Takenaka, T. (1995b) Distribution of galanin-immunoreactive nerve fibers in the carotid labyrinth of the bullfrog,Rana catesbeiana: comparison with substance P-immunoreactive fibers.Cell Tissue Res. 281, 63–7.PubMedGoogle Scholar
  18. Lundberg, J.M., Hökfelt, T., Anggard, A., Pernow, B. &Emson, P. (1979) Immunohistochemical evidence for substance P immunoreactive nerve fibers in the taste buds of the cat.Acta Physiol. Scand. 107, 389–91.PubMedGoogle Scholar
  19. Lundberg, J.M., Franco-Cereceda Hua, X., Hökfelt, T. &Fischer, A. (1985) Co-existence of substance P and calcitonin generelated peptide-like immunoreactivities in sensory nerves in relation to cardiovascular and bronchoconstrictor effects of capsaicin.Eur. J. Pharmacol. 108, 315–19.CrossRefPubMedGoogle Scholar
  20. Luts, A., Montavon, P., Lindstrand, K. &Sundler, F. (1990) Peptide-containing nerve fibers in the circumvallate papillae.Regul. Pep. 27, 209–26.CrossRefGoogle Scholar
  21. Montavon, P., Lindstrand, K., Luts, A. &Sundler, F. (1991) Peptide-containing nerve fibers in the fungiform papillae of pigs and rats.Regul. Pep. 32, 141–50.Google Scholar
  22. Murray, R.G. (1973) The ultrastructure of taste buds. InThe Ultrastructure of Sensory Organs (edited by J. Friedmann) pp. 1–39. Amsterdam: North-Holland.Google Scholar
  23. Nagy, J.I., Goedert, M., Hunt, A.P. &Bond A. (1982) The nature of substance P-containing nerve fibers in taste papillae of the rat tongue.Neuroscience 7, 3137–51.PubMedGoogle Scholar
  24. Nishimoto, T., Araki, M., Inagaki, S., Shiosaka, S., Shimizu, Y., Yamamoto, K., Senba, E., Sakanaka, M., Takasuki, K., Hara, Y., Takagi, H., Matsuzaki, T. &Tohyama, M. (1982) On the distribution and origins of substance P in the papillae of the rat tongue: an experimental and immunohistochemical study.J. Comp. Neurol. 207, 85–92.CrossRefPubMedGoogle Scholar
  25. Rapuzzi, G. &Casella, C. (1965) Innervation of the fungiform papillae in the frog tongue.J. Neurophysiol. 28, 154–65.PubMedGoogle Scholar
  26. Rosenfeld, M.G., Mermod, J.-J., Amara, S.G., Swanson, L.W., Sawchenko, P.E., Rivier, J., Vale, W.W. &Evans, R.M. (1983) Production of a novel neuropeptide encoded by the calcitonin gene via tissue-specific RNA processing.Nature 304, 129–35.CrossRefPubMedGoogle Scholar
  27. Stensaas, L.J. (1971) The fine structure of fungiform papillae and epithelium of the tongue of South American toad,Calyptocephalella gayi.Am. J. Anat. 131, 443–62.CrossRefPubMedGoogle Scholar
  28. Sundler, F., Brodin, E., Ekblad, E., Hakanson, R. &Uddman, R. (1985) Sensory nerve fibers: distribution of substance P, neurokinin A and calcitonin gene-related peptide. InTachykinin Antagonists (edited by R. Håkanson & F. Sundler), pp. 3–14. Amsterdam: Elsevier.Google Scholar
  29. Terenghi, G., Polak, J.M., Rodrigo, J., Mulderry, P.K. &Bloom, S.R. (1986) Calcitonin gene-related peptide-immunoreactive nerves in the tongue, epiglotis and pharynx of the rat: occurrence, distribution and origin.Brain Res. 365, 1–14.CrossRefPubMedGoogle Scholar
  30. Uga, S. &Hama, K. (1967) Electron microscopic studies on the synaptic region of the taste organ of carps and frogs.J. Electronmicrosc. 16, 269–76.Google Scholar
  31. Yamasaki, H., Kubota, Y., Takagi, H. &Tohyama, M. (1984) Immunoelectronmicroscopic study of the fine structure of substance P-containing fibers in the taste buds of the rat.J. Comp. Neurol. 227, 380–93.CrossRefPubMedGoogle Scholar
  32. Yamasaki, H., Kubota, Y. &Tohyama, M. (1985) Ontogeny of substance P-containing fibers in the taste buds and surrounding epithelium. I. Light microscopic analysis.Dev. Brain Res. 18, 301–5.CrossRefGoogle Scholar
  33. Zamboni, L. &Demartino, C. (1967) Buffered picric acid formaldehyde: a new rapid fixative for electron microscopy.J. Cell Biol. 35, 148A.Google Scholar

Copyright information

© Chapman & Hall 1996

Authors and Affiliations

  • Tatsumi Kusakabe
    • 1
  • Tadashi Kawakami
    • 2
  • Michio Ono
    • 1
  • Hajime Sawada
    • 1
  • Toshifumi Takenaka
    • 2
  1. 1.Department of AnatomyYokohama City University School of MedicineYokohamaJapan
  2. 2.Department of PhysiologyYokohama City University School of MedicineYokohamaJapan

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